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Genetic Diversity of the Cryptococcus gattii Species Complex in Mato Grosso State, Brazil

  • Fernanda Harumi MaruyamaEmail author
  • Daphine Ariadne Jesus de Paula
  • Isabela de Godoy Menezes
  • Olívia Cometti Favalessa
  • Rosane Christine Hahn
  • Arleana do Bom Parto Ferreira de Almeida
  • Valéria Régia Franco Sousa
  • Luciano Nakazato
  • Valéria Dutra
Short Communication
  • 26 Downloads

Abstract

Cryptococcosis is caused by fungi of the genus Cryptococcus. Owing to its importance, this study aimed to analyze the genetic diversity of C. gattii isolates from animals, humans, and the environment in Mato Grosso State (MT), Brazil, during November 2010–December 2017. All isolates of the C. gattii species complex were subjected to molecular genotyping via Restriction Fragment Length Polymorphism (PCR–RFLP) and Multi-locus Sequence Typing (MLST). PCR–RFLP analysis revealed that 21 isolates presented the genotype VGII, which is considered the most common and virulent genotype globally among. MLST analysis revealed the presence of 14 sequence types (STs), of which 5 are considered new genotypes. Clonal Complex (CC) CC182 (n = 5; 23,80%) and CC309 (n = 3; 14,28%) were the most frequent. CC distribution in relation to origin revealed that three CCs were found in animals with a predominance of CC182 (66,66%), while nine were found in humans, and two CCs were found in the environment. Extensive genetic variability was observed among the isolates in the State of Mato Grosso. STs belonging to the already described clonal complexes (CC) indicate the global expansion and adaptation of isolates in several other countries. Therefore, detection of clonal complexes and STs already described in other regions and the occurrence of new STs in the present study help further the current understanding of the geographic dispersion and genetic origin of the C. gattii species complex.

Keywords

Cryptococcus gattii Multi-locus sequence typing Genotyping Cryptococcosis 

Notes

Acknowledgements

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical Approval

This study was certificated of the Animal and Human Ethics Committee No. 888/CEP-HUJM/2012.

References

  1. 1.
    Rajasingham R, Smith RM, Park BJ, Jarvis JN, Govender NP, Chiller TM, et al. Global burden of disease of HIB-associated cryptococcal meningitis: na updated analysis. Lancet Infect Dis. 2017;17:873–81.  https://doi.org/10.1016/S1473-3099.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Singer LM, Meyer W, Firacative C, Thompson GR, Samitz E, Sykes JE. Antifungal drug susceptibility and phylogenetic diversity among Cryptococcus isolates from dogs and cats in North America. J Clin Microbiol. 2014;52:2061–70.  https://doi.org/10.1128/JCM.03392-13.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Hagen F, Khayhan K, Theelen B, Kolecka A, Polacheck I, Sionov E, et al. Recognition of seven species in the Cryptococcus gattii/Cryptococcus neoformans species complex. Fungal Genet Biol. 2015;78:16–48.  https://doi.org/10.1016/j.fgb.2015.02.009.CrossRefPubMedGoogle Scholar
  4. 4.
    Kwon-Chung KJ, Bennett JE, Wickes BL, Meyer W, Cuomo CA, Wollenburg KR, Bicanic TA, et al. The case for adopting the “species complex” nomenclature for the etiologic agents of cryptococcosis. mSphere. 2017;2:e00357-16.  https://doi.org/10.1128/msphere.00357-16.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Harris J, Lockhart S, Chiller T. Cryptococcus gattii: Where do we go from here? Med Mycol. 2012;50:113–29.  https://doi.org/10.3109/13693786.2011.607854.CrossRefPubMedGoogle Scholar
  6. 6.
    Kwon-Chung KJ, Fraser JA, Doering TL, Wang ZA, Janbon G, Idnurm A, et al. Cryptococcus neoformans and Cryptococcus gattii, the etiologic agents of cryptococcosis. Cold Spring Harb Perspect Med. 2014;4:1–27.  https://doi.org/10.1101/cshperspect.a019760.CrossRefGoogle Scholar
  7. 7.
    Stephen C, Lester S, Black W, Fyfe M, Raverty S. Multispecies outbreak of cryptococcosis on southern Vancouver Island, British Columbia. Can Vet J. 2002;43:792–4.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Espinel-Ingroff A, Kidd SE. Current trends in the prevalence of Cryptococcus gattii in the United States and Canada. Infect Drug Resist. 2015;8:89–97.  https://doi.org/10.2147/IDR.S57686.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Shields AB, Ajello L. Medium for selective isolation of Cryptococcus neoformans. Science. 1966;151:208–9.CrossRefGoogle Scholar
  10. 10.
    Del Poeta M, Toffaletti DN, Rude TH, Dykstra CC, Heitamn J, Perfec JR. Topoisomerase I is essential in Cryptococcus neoformans: role in pathobiology and as an antifungal target. Genet Soc Am. 1999;152:167–78.Google Scholar
  11. 11.
    Aoki FH, Imai T, Tanaka R, Mikami Y, Taguchi H, Nishimura NF, et al. New PCR primer pairs specific for Cryptococcus neoformans serotype A or B prepared on the basis of random amplified polymorphic DNA fingerprint pattern analyses. J Clin Microbiol. 1999;37:315–20.PubMedPubMedCentralGoogle Scholar
  12. 12.
    D’Souza C, Hagen F, Boekhout T, Cox GM, Heitman J. Investigation of the basis of virulence in serotype A strains of Cryptococcus neoformans from apparently immunocompetent individuals. Curr Genet. 2004;46:92–102.  https://doi.org/10.1007/s00294-004-0511-y.CrossRefPubMedGoogle Scholar
  13. 13.
    Meyer W, Castañeda A, Jackso S, Huynh M, Castañeda E, I.C.S. Group. Molecular typing of IberoAmerican Cryptococcus neoformans isolates. Emerg Infect Dis. 2003;9:189–95.  https://doi.org/10.3201/eid0902.020246.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Meyer W, Aanensen DM, Boekhout T, Cogliati M, Diaz MR, Esposto MC, et al. Consensus multi-locus sequence typing scheme for Cryptococcus neoformans and Cryptococcus gattii. Med Mycol. 2009;47:561–70.  https://doi.org/10.1080/13693780902953886.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Dou HT, Xu YC, Wang HZ, Li TS. Molecular epidemiology of Cryptococcus neoformans and Cryptococcus gattii in China between 2007 and 2013. Eur J Clin Microbiol Infect Dis. 2015;34:753–63.  https://doi.org/10.1007/s10096-014-2289-2.CrossRefPubMedGoogle Scholar
  16. 16.
    Chen SC, Meyer W, Sorrell TC. Cryptococcus gattii infections. Clin Microbiol Rev. 2014;27:980–1024.  https://doi.org/10.1128/CMR.00126-13.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Springer DJ, Chatuverdi V. Projecting global occurrence of Cryptococcus gattii. Emerg Infect Dis. 2010;16:14–20.  https://doi.org/10.3201/eid1601.090369.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Hagen F, Ceresini PC, Polacheck I, Ma H, Nieuwerburgh FV, Gabaldón T, et al. Ancient dispersal of the human fungal pathogen Cryptococcus gattii from the Amazon rainforest. PLoS ONE. 2013;8:e71148.  https://doi.org/10.1371/journal.pone.0071148.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Kidd SE, Hagen F, Tscharke RL, Huynh M, Bartlett KH, Fyfe M, et al. A rare genotype of Cryptococcus gattii caused the cryptococcosis outbreak on Vancouver Island (British Columbia, Canada). Proc Natl Acad Sci USA. 2004;101:17258–63.  https://doi.org/10.1073/pnas.0402981101.CrossRefPubMedGoogle Scholar
  20. 20.
    Feng X, Yao Z, Ren D, Liao W, Wu J. Genotype and mating type analysis of Cryptococcus neoformans and Cryptococcus gattii isolates from China that mainly originated from non-HIV-infected patients. FEMS Yeast Res. 2008;8:930–8.  https://doi.org/10.1111/j.1567-1364.2008.00422.x.CrossRefPubMedGoogle Scholar
  21. 21.
    Ngamskulrungroj P, Gilgado F, Faganello J, Litvintseva AP, Leal AL, Tsui KM. Genetic diversity of the Cryptococcus species complex suggests that Cryptococcus gattii deserves to have varieties. PLoS ONE. 2009;4:e5862.  https://doi.org/10.1371/journal.pone.0005862.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Trilles L, Lázera MS, Wanke B, Oliveira RV, Barbosa GG, Nishikawa MM, et al. Regional pattern of the molecular types of C. neoformans and C. gattii in Brazil. Memoria Instituto Oswaldo Cruz. 2008;103:455–62.CrossRefGoogle Scholar
  23. 23.
    Casali AK, Goulart L, Silva LKR, Ribeiro AM, Amaral AA, Alves SH, et al. Molecular typing of clinical and environmental Cryptococcus neoformans isolates in the Brazilian state Rio Grande do Sul. FEMS Yeast Res. 2003;3:405–15.  https://doi.org/10.1016/S1567-1356(03)00038-2.CrossRefPubMedGoogle Scholar
  24. 24.
    Paula DAJ, Almeida ABPF, Cruz FS, Furlan FH, Colodel EM, Sousa VRF, et al. Occurrence and molecular characterization of cryptococcosis in dogs and cats in Mato Grosso, Brazil. Pesquisa Veterinária Brasileira. 2014;34:167–72.CrossRefGoogle Scholar
  25. 25.
    Souto ACP, Bonfietti LX, Ferreira-Paim K, Trilles L, Martins M, Ribeiro-Alves M, et al. Population genetic analysis reveals a high genetic diversity in the brazilian Cryptococcus gattii VGII population and shifts the global origin from the amazon rainforest to the semi-arid desert in the northeast of Brazil. PLOS Negl Trop Dis. 2016;10:1–19.  https://doi.org/10.1371/journal.pntd.0004885.CrossRefGoogle Scholar
  26. 26.
    Silva EC, Guerra JM, Torres LN, Lacerda AMD, Gomes RG, Rodrigues DM, et al. Cryptococcus gattii molecular type VGII infection associated with lung disease in a goat. BMC Vet Res. 2017;13:1–6.  https://doi.org/10.1186/s12917-017-0950-6.CrossRefGoogle Scholar
  27. 27.
    Barcellos VA, Martins LMS, Fontes ACL, Rewsaat JCV, Squizani WD, Araújo GRS, et al. Genotypic and phenotypic diversity of Cryptococcus gattii VGII clinical isolates and its impact on virulence. Front Microbiol. 2018;9:132.  https://doi.org/10.3389/fmicb.2018.00132.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Lockhart SR, Igbal N, Harris JR, Grossman NT, Debess E, Wohrle R, et al. Cryptococcus gattii in the United States: genotypic diversity of human and veterinary isolates. PLoS ONE. 2013;8:e74737.  https://doi.org/10.1371/journal.pone.0074737.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Herck HV, Ingh TSGAMVD, Hage MHVD, Zwart P. Dermal cryptococcosis in a guineapig. Lab Anim. 1988;22:88–91.CrossRefGoogle Scholar
  30. 30.
    Bonfietti LX, Pham CD, Szeszs MW, Silva DC, Martins MA, Lockhart SR, et al. Diversidade de isolados clínicos de Cryptococcus gattii por multi-locus sequence typing no Estado de São Paulo. Boletim do Instituto Adolfo Lutz. 2014;24:36–9.Google Scholar
  31. 31.
    Carriconde F, Gilgado F, Arthur I, Ellis D, Malik R, Wiele NV, et al. Clonality and a—a recombination in the Australian Cryptococcus gattii VGII population—an emerging outbreak in Australia. PLoS ONE. 2011;6:e16936.  https://doi.org/10.1371/journal.pone.0016936.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Brito-Santos F, Barbosa GG, Trilles L, Nishikawa MM, Wanke B, Meyer W, et al. Environmental isolation of Cryptococcus gattii VGII from indoor dust from typical wooden houses in the deep Amazonas of the Rio Negro basin. PLoS ONE. 2015;10:e0115866.  https://doi.org/10.1371/journal.pone.0115866.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Engelthaler DM, Hicks ND, Gillece JD, Roe CC, Schupp JM, Driebe EM, et al. Cryptococcus gattii in North American Pacific Northwest: whole-population genome analysis provides insights into species evolution and dispersal. MBio. 2014;5:e0146414.  https://doi.org/10.1128/mBio.01464-14.CrossRefGoogle Scholar
  34. 34.
    Lizazaro J, Escandón P, Agudelo CI, Firacative C, Meyer W, Castañeda E. Retrospective study of the epidemiology and clinical manifestations of Cryptococcus gattii infections in Colombia from 1997 to 2011. PLoS Negl Trop Dis. 2014;8:e3272.  https://doi.org/10.1371/journal.pntd.0003272.CrossRefGoogle Scholar
  35. 35.
    Alves GSB, Freire AKL, Bentes AS, Pinheiro JFS, Souza JVB, Wanke B. Original article molecular typing of environmental Cryptococcus neoformans/C. gattii species complex isolates from Manaus, Amazonas, Brazil. Mycoses. 2016;59:509–15.  https://doi.org/10.1111/myc.12499.CrossRefPubMedGoogle Scholar
  36. 36.
    Hagen F, Colom MF, Swinne D, Tintelnot K, Iatta R, Montagna MT, et al. Autochthonous and dormant Cryptococcus gattii infections in Europe. Emerg Infect Dis. 2012;18:1618–24.  https://doi.org/10.3201/eid1810.120068.CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    IBGE. Mapas de biomas do Brasil: escala 1:5.000.000. 2017. Disponível em. http://mapas.ibge.gov.br/biomas2/viewer.htm. Acesso em 02 maio 2017.

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Fernanda Harumi Maruyama
    • 1
    Email author
  • Daphine Ariadne Jesus de Paula
    • 1
  • Isabela de Godoy Menezes
    • 1
  • Olívia Cometti Favalessa
    • 2
  • Rosane Christine Hahn
    • 2
  • Arleana do Bom Parto Ferreira de Almeida
    • 1
  • Valéria Régia Franco Sousa
    • 1
  • Luciano Nakazato
    • 1
  • Valéria Dutra
    • 1
  1. 1.Postgraduate Course in Veterinary Sciences, Department of Veterinary SciencesFederal University of Mato GrossoCuiabáBrazil
  2. 2.Postgraduate Course in Health Sciences, Department of Molecular BiologyFederal University of Mato GrossoCuiabáBrazil

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